Dissection of the genetic architecture of adaptation and abiotic stress-related traits is highly desirable for developing drought-tolerant potatoes and enhancing the resilience of existing cultivars, particularly as agricultural production in rain-fed areas may be reduced by up to 50 % by 2020. The “DMDD” potato progeny was developed at International Potato Center (CIP) by crossing the sequenced double monoploid line DM and a diploid cultivar of the Solanum tuberosum diploid Andigenum Goniocalyx group. Recently, a high-density integrated genetic map based on single nucleotide polymorphism (SNP), diversity array technology (DArT), simple sequence repeats (SSRs), and amplified fragment length polymorphism (AFLP) markers was also made available for this population. Two trials were conducted, in greenhouse and field, for drought tolerance with two treatments each, well-watered and terminal drought, in which watering was suspended 60 days after planting. The DMDD population was evaluated for agro-morphological and physiological traits before and after initiation of stress, at multiple time points. Two dense parental genetic maps were constructed using published genotypic data, and quantitative trait locus (QTL) analysis identified 45 genomic regions associated with nine traits in well-watered and terminal drought treatments and 26 potentially associated with drought stress. In this study, the strong influence of environmental factors besides water shortage on the expression of traits and QTLs reflects the multigenic control of traits related to drought tolerance. This is the first study to our knowledge in potato identifying QTLs for drought-related traits in field and greenhouse trials, giving new insights into genetic architecture of drought-related traits. Many of the QTLs identified have the potential to be used in potato breeding programs for enhanced drought tolerance.